3D electron microscopy of biological nanomachines: Principles and applications

European Biophysics Journal

Volumn 36, Issue 8, 2007, Pages 995-1013

  Sorzano, C O S ^a   Jonic, S ^b   Cottevieille, M ^b   Larquet, E ^b   Boisset, N ^b   Marco, S ^c,d  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

^b UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^c INSTITUT CURIE   (France)

^d Centre Universitaire   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; GLUTAMATE SYNTHASE;

COMPUTER AIDED DESIGN; CRYSTALLOGRAPHY; ENZYME STRUCTURE; FOURIER ANALYSIS; GEOMETRY; METHODOLOGY; NANOTECHNOLOGY; REVIEW; STRUCTURE ANALYSIS; TOMOGRAPHY; TRANSMISSION ELECTRON MICROSCOPY;

ALGORITHMS; IMAGING, THREE-DIMENSIONAL; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR CONFORMATION;

EID: 35748956741     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-007-0203-x     Document Type: Review

References (208)

1. Adrian M, Dubochet J, Fuller SD, Harris JR (1998) Cryo-negative staining. Micron 29:145-160
2. Al-Amoudi A, Chang JJ, Leforestier A, McDowall A, Salamin LM, Norlen LP, Richter K, Blanc NS, Studer D, Dubochet J (2004) Cryo-electron microscopy of vitreous sections. Embo J 23:3583-3588
3. Al-Amoudi A, Dubochet J, Gnaegi H, Luthi W, Studer D (2003) An oscillating cryo-knife reduces cutting-induced deformation of vitreous ultrathin sections. J Microsc 212:26-33
4. Aramayo R, Merigoux C, Larquet E, Bron P, Perez J, Dumas C, Vachette P, Boisset N (2005) Divalent ion-dependent swelling of tomato bushy stunt virus: a multi-approach study. Biochim Biophys Acta 1724:345-354
5. Baker D, Sali A (2001) Protein structure prediction and structural genomics. Science 294:93-96
6. Baker TS, Cheng RH (1996) A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J Struct Biol 116:120-130
7. Baker TS, Olson NH, Fuller SD (1999) Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol Mol Biol 63:862-922
8. Baumeister W, Steven AC (2000) Macromolecular electron microscopy in the era of structural genomics. Trends Biochem Sci 25:624-631
9. Berry IM, Dym O, Esnouf RM, Harlos K, Meged R, Perrakis A, Sussman JL, Walter TS, Wilson J, Messerschmidt A (2006) SPINE high-throughput crystallization, crystal imaging and recognition techniques: current state, performance analysis, new technologies and future aspects. Acta Crystallogr D Biol Crystallogr 62:1137-1149
10. Binda C, Bossi RT, Wakatsuki S, Arzt S, Coda A, Curti B, Vanoni MA, Mattevi A (2000) Cross-talk and ammonia channeling between active centers in the unexpected domain arrangement of glutamate synthase. Structure 8:1299-1308
11. Bluemke DA, Carragher B, Josephs R (1988) The reconstruction of helical particles with variable pitch. Ultramicroscopy 26:255-270
12. Böhm J, Frangakis AS, Hegerl R, Nickell S, Typke D, Baumeister W (2000) Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. Proc Natl Acad Sci USA 97:14245-14250
13. Boisset N, Penczek P, Taveau JC, You V, Haas Fd, Lamy J (1998) Overabundant single-particle electron microscope views induce a three-dimensional reconstruction artifact. Ultramicroscopy 74:201-207
14. Boudier T, Lechaire JP, Frebourg G, Messaoudi C, Mory C, Colliex C, Gaill F, Marco S (2005) A public software for energy filtering transmission electron tomography (EFTET-J): application to the study of granular inclusions in bacteria from Riftia pachyptila. J Struct Biol 151:151-159
15. Boutselakis H, Dimitropoulos D, Fillon J, Golovin A, Henrick K, Hussain A, Ionides J, John M, Keller PA, Krissinel E, McNeil P, Naim A, Newman R, Oldfield T, Pineda J, Rachedi A, Copeland J, Sitnov A, Sobhany S, Suarez-Uruena A, Swaminathan J, Tagari M, Tate J, Tromm S, Velankar S, Vranken W (2003) E-MSD: the European bioinformatics institute macromolecular structure database. Nucleic Acids Res 31:458-462
16. Brandt S, Heikkonen J, Engehardt P (2001a) Automatic alignment of transmission electron microscope tilt series without fiducial markers. J Struct Biol 136:201-213
17. Brandt S, Heikkonen J, Engehardt P (2001b) Multiphase method for automatic alignment of transmission electron microscope images using markers. J. Struct Biol 133:10-22
18. Brink J, Ludtke SJ, Kong Y, Wakil SJ, Ma J, Chiu W (2004) Experimental verification of conformational variation of human fatty acid synthase as predicted by normal mode analysis. Structure 12:185-191
19. Broersen PMT (2000) Facts and fiction in spectral analysis. IEEE Trans Instrum Meas 49:766-772
20. Carragher B, Whittaker M, Milligan RA (1996) Helical processing using PHOELIX. J Struct Biol 116:107-112
21. Conway JF, Steven AC (1999) Methods for reconstructing density maps of "single" particles from cryoelectron micrographs to subnanometer resolution. J Struct Biol 128:106-118
22. Crowther RA (1971) Procedures for three-dimensional reconstruction of spherical viruses by Fourier synthesis from electron micrographs. Philos Trans R Soc Lond B Biol Sci 261:221-230
23. Crowther RA, Amos LA, Finch JT, Rosier DJD, Klug A (1970) Three dimensional reconstructions of spherical viruses by fourier synthesis from electron micrographs. Nature 226:421-425
24. Crowther RA, Henderson R, Smith JM (1996) MRC image processing programs. J Struct Biol 116:9-16
25. De Carlo S, El-Bez C, Alvarez-Rua C, Borge J, Dubochet J (2002) Cryo-negative staining reduces electron-beam sensitivity of vitrified biological particles. J Struct Biol 138:216-226
26. Defrise M (2001) A short reader's guide to 3D tomographic reconstruction. Comput Med Imaging Graph 25:113-116
27. DeRosier D, Klug A (1968) Reconstruction of three-dimensional structures from electron micrographs. Nature 217:130-134
28. DeRosier DJ, Moore PB (1970) Reconstruction of three-dimensional images from electron micrographs of structures with helical symmetry. J Mol Biol 52:355-369
29. Dierksen K, Typke D, Hegerl R, Koster AJ, Baumeister W (1992) Towards automatic electron tomography. Ultramicroscopy 40:71-87
30. Dimmeler E, Marabini R, Tittmann P, Gross H (2001) Correlation of topographic surface and volume data from 3D electron microscopy. J Struct Biol 136:20-29
31. Dippell R (1968) The development of basal bodies in paramecium. Proc Natl Acad Sci USA 61:461-468
32. Dippell R (1976) Effect of nuclease and protease digestion on the ultrastructure of Paramecium basal bodies. J Cell Biol 69:622-637
33. Dobritzsch D, Schneider G, Schnackerz KD, Lindqvist Y (2001) Crystal structure of dihydropyrimidine dehydrogenase, a major determinant of the pharmacokinetics of the anti-cancer drug 5-fluorouracil. Embo J 20:650-660
34. Dubochet J (1995) High-pressure freezing for cryoelectron microscopy. Trends Cell Biol 5:366-368
35. Dubochet J, Lepault J, Freeman R, Berriman JA, Homo JC (1982) Electron microscopy of frozen water and aqueous solutions. J Microsc 128:219-237
36. Dubochet J, Sartori Blanc N (2001) The cell in absence of aggregation artifacts. Micron 32:91-99
37. Dute R, Kung C (1978) Ultrastructure of the proximal region of somatic cilia in Paramecium tetraurelia. J Cell Biol 78:451-464
38. Egelman EH (1986) An algorithm for straightening images of curved filamentous structures. Ultramicroscopy 19:367-373
39. Egelman EH (2007) The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J Struct Biol 157:83-94
40. Egerton RF, Li P, Malac M (2004) Radiation damage in the TEM and SEM. Micron 35:399-409
41. Ellis MJ, Hebert H (2001) Structure analysis of soluble proteins using electron crystallography. Micron 32:541-550
42. Engel A, Muller DJ (2000) Observing single biomolecules at work with the atomic force microscope. Nat Struct Biol 7:715-718
43. Falke S, Tama F, Brooks CL 3rd, Gogol EP, Fisher MT (2005) The 13 Å structure of a chaperonin GroEL-protein substrate complex by cryo-electron microscopy. J Mol Biol 348:219-230
44. Fernandez JJ, Sanjurjo JR, Carazo JM (1997) A spectral estimation approach to contrast transfer function detection in electron microscopy. Ultramicroscopy 68:267-295
45. Fernandez JJ, Sorzano COS, Marabini R, Carazo JM (2006) Image processing and 3-D reconstruction in electron microscopy. IEEE Signal Process Mag 23:84-94
46. Fotin A, Kirchhausen T, Grigorieff N, Harrison SC, Walz T, Cheng Y (2006) Structure determination of clathrin coats to subnanometer resolution by single particle cryo-electron microscopy. J Struct Biol 156:453-460
47. Frangakis AS, Bohm J, Forster F, Nickell S, Nicastro D, Typke D, Hegerl R, Baumeister W (2002) Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc Natl Acad Sci USA 99:14153-14158
48. Frank J (2002) Single-particle imaging of macromolecules by cryo-electron microscopy. Annu Rev Biophys Biomol Struct 31:303-319
49. Frank J (2006) Three-dimensional electron microscopy of macromolecular assemblies: visualization of biological molecules in their native state. Oxford University Press, New York
50. Frank J, Penczek PA (1995) On the correction of the contrast transfer function in biological electron microscopy. Optik 98:125-129
51. Frank J, Radermacher M, Penczek P, Zhu J, Li Y, Ladjadj M, Leith A (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116:190-199
52. Frank J, Verschoor A, Boublik M (1981) Computer averaging of electron micrographs of 40S ribosomal subunits. Science 214:1353-1355
53. Fuller SD, Butcher SJ, Cheng RH, Baker TS (1996) Three-dimensional reconstruction of icosahedral particles-the uncommon line. J Struct Biol 116:48-55
54. Gabashvili IS, Agrawal RK, Spahn CM, Grassucci RA, Svergun DI, Frank J, Penczek P (2000) Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100:537-549
55. Gao H, Valle M, Ehrenberg M, Frank J (2004) Dynamics of EF-G interaction with the ribosome explored by classification of a heterogeneous cryo-EM dataset. J Struct Biol 147:283-290
56. Gelfand MS, Goncharov AB (1990) Spatial rotational alignment of identical particles given their projections: theory and practice. Transl Math Monogr 81:97-122
57. Gil D, Carazo JM, Marabini R (2006) On the nature of 2D crystal unbending. J Struct Biol 156:546-555
58. Gilbert P (1972) Iterative methods for the three-dimensional reconstruction of an object from projections. J Theor Biol 36:105-117
59. Gipson B, Zeng X, Zhang ZY, Stahlberg H (2007) 2dx-user-friendly image processing for 2D crystals. J Struct Biol 157:64-72
60. Glaeser RM (1971) Limitations to significant information in biological electron microscopy as a result of radiation damage. J Ultrastruct Res 36:466-482
61. Glaeser RM (1999) Review: electron crystallography: present excitement, a nod to the past, anticipating the future. J Struct Biol 128:3-14
62. Goncharov AB (1990) Three-dimensional reconstruction of arbitrarily arranged identical particles given their projections. Transl Math Monogr 81:67-95
63. Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, Harrison SC, Walz T (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438:633-638
64. Grigorieff N (1998) Three-dimensional structure of bovine NADH: ubiquinone oxidoreductase (complex I) at 22 A in ice. J Mol Biol 277:1033-1046
65. Grigorieff N (2007) FREALIGN: high-resolution refinement of single particle structures. J Struct Biol 157:117-125
66. Grunewald K, Cyrklaff M (2006) Structure of complex viruses and virus-infected cells by electron cryo tomography. Curr Opin Microbiol 9:437-442
67. Grunewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, Baumeister W, Steven AC (2003) Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302:1396-1398
68. Gue M, Marco S, Croissy A, Rigaud JL, Boudier T (2005) Integrative imaging: a new challenge for cell biology. Imaging Microsc 7:51-53
69. Hamada D, Higurashi T, Mayanagi K, Miyata T, Fukui T, Iida T, Honda T, Yanagihara I (2007) Tetrameric structure of thermostable direct hemolysin from vibrio parahaemolyticus revealed by ultracentrifugation, small-angle X-ray scattering and electron microscopy. J Mol Biol 365:187-195
70. Harauz G, van Heel M (1986) Exact filters for general geometry three dimensional reconstruction. Optik 73:146-156
71. Henderson R (2004) Realizing the potential of electron cryo-microscopy. Q Rev Biophys 37:3-13
72. Herman GT (1980) Image reconstruction from projections: the fundamentals of computerized tomography. Academic, New York
73. Herman GT (1998) Algebraic reconstruction techniques in medical imaging. In: Leondes CT (ed) Medical imaging, systems techniques and applications: computational techniques, vol 6. Gordon and Breach Science Publishers, Amsterdam, pp 1-42
74. Herman GT, Lent A, Rowland SW (1973) ART: mathematics and applications. A report on the mathematical foundations and on the applicability to real data of the algebraic reconstruction techniques. J Theor Biol 42:1-32
75. Heymann JB, Belnap DM (2007) Bsoft: image processing and molecular modeling for electron microscopy. J Struct Biol 157:3-18
76. Heymann JB, Chagoyen M, Belnap DM (2005) Common conventions for interchange and archiving of three-dimensional electron microscopy information in structural biology. J Struct Biol 151:196-207
77. Hoppe W, Hegerl R (1980) Three-dimensional structure determination by electron microscopy (nonperiodic specimens). In: Hawkes PW (ed) Computer processing of electron microscope images, vol 13. Springer-Verlag, Berlin, pp 127-183
78. Hsieh CE, Marko M, Frank J, Mannella CA (2002) Electron tomographic analysis of frozen-hydrated tissue sections. J Struct Biol 138:63-73
79. Huang Z, Baldwin PR, Mullapudi S, Penczek PA (2003) Automated determination of parameters describing power spectra of micrograph images in electron microscopy. J Struct Biol 144:79-94
80. Jones DT (2001) Protein structure prediction in genomics. Brief Bioinform 2:111-125
81. Jonic S, Sorzano CO, Cottevieille M, Larquet E, Boisset N (2007) A novel method for improvement of visualization of power spectra for sorting cryo-electron micrographs and their local areas. J Struct Biol 157:156-167
82. Jonic S, Sorzano CO, Thevenaz P, El-Bez C, De Carlo S, Unser M (2005) Spline-based image-to-volume registration for three-dimensional electron microscopy. Ultramicroscopy 103:303-317
83. Kak AC, Slaney M (1988) Principles of computerized tomographic imaging. IEEE Press, New York
84. Klug A, Crick FHC, Wyckoff HW (1958) Diffraction by helical structures. Acta Crystallogr 11:199-213
85. Koster AJ, Chen H, Sedat JW, Agard D (1992) Automated microscopy for electron tomography. Ultramicroscopy 46:207-227
86. Koster AJ, Klumperman J (2003) Electron microscopy in cell biology: integrating structure and function. Nat Cell Biol Suppl S:SS6-SS10
87. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-76
88. Lanzavecchia S, Cantele F, Bellon PL, Zampighi L, Kreman M, Wright E, Zampighi GA (2005) Conical tomography of freeze-fracture replicas: a method for the study of integral membrane proteins inserted in phospholipid bilayers. J Struct Biol 149:87-98
89. Le Gros MA, McDermott G, Larabell CA (2005) X-ray tomography of whole cells. Curr Opin Struct Biol 15:593-600
90. Leapman RD (2004) Novel techniques in electron microscopy. Curr Opin Neurobiol 14:591-598
91. Leapman RD, Kocsis E, Zhang G, Talbot TL, Laquerriere P (2004) Three-dimensional distributions of elements in biological samples by energy-filtered electron tomography. Ultramicroscopy 100:115-125
92. Lee KK, Johnson JE (2003) Complementary approaches to structure determination of icosahedral viruses. Curr Opin Struct Biol 13:558-569
93. Lei J, Frank J (2005) Automated acquisition of cryo-electron micrographs for single particle reconstruction on an FEI Tecnai electron microscope. J Struct Biol 150:69-80
94. Lepault J, Dubochet J (1986) Electron microscopy of frozen hydrated specimens: preparation and characteristics. Methods Enzymol 127:719-730
95. Leschziner AE, Nogales E (2006) The orthogonal tilt reconstruction method: an approach to generating single-class volumes with no missing cone for ab initio reconstruction of asymmetric particles. J Struct Biol 153:284-299
96. Leschziner AE, Nogales E (2007) Visualizing flexibility at molecular resolution: analysis of heterogeneity in single-particle electron microscopy reconstructions. Ann Rev Biophys Biomol Struct 36:43-62
97. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128:82-97
98. Ludtke SJ, Chen DH, Song JL, Chuang DT, Chiu W (2004) Seeing GroEL at 6 Å resolution by single particle electron cryomicroscopy. Structure 12:1129-1136
99. Mallick SP, Carragher B, Potter CS, Kriegman DJ (2005) ACE: automated CTF estimation. Ultramicroscopy 104:8-29
100. Marabini R, Herman GT, Carazo JM (1998) 3D reconstruction in electron microscopy using ART with smooth spherically symmetric volume elements (blobs). Ultramicroscopy 72:53-65
101. Marabini R, Rietzel E, Schröder R, Herman GT, Carazo JM (1997) Three-dimensional reconstruction from reduced sets of very noisy images acquired following a single-axis tilt schema: application of a new three-dimensional reconstruction algorithm and objective comparison with weighted backprojection. J Struct Biol 120:363-371
102. Marabini R, Sorzano COS, Matej S, Fernandez JJ, Carazo JM, Herman GT (2004) 3D reconstruction of 2D crystals. IEEE Trans Image Process 13:549-561
103. Martin AG, Depoix F, Stohr M, Meissner U, Hagner-Holler S, Hammouti K, Burmester T, Heyd J, Wriggers W, Markl J (2007) Limulus polyphemus hemocyanin: 10 A cryo-EM structure, sequence analysis, molecular modelling and rigid-body fitting reveal the interfaces between the eight hexamers. J Mol Biol 366:1332-1350
104. Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120:343-352
105. Matias VR, Al-Amoudi A, Dubochet J, Beveridge TJ (2003) Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185:6112-6118
106. Matricardi VR, Moretz RC, Parsons DF (1972) Electron diffraction of wet proteins: catalase. Science 177:268-270
107. Messaoudi C, Boudier T, Lechaire JP, Rigaud JL, Delacroix H, Gaill F, Marco S (2003) Use of cryo-negative staining in tomographic reconstruction of biological objects: application to T4 bacteriophage. Biol Cell 95:393-398
108. Messaoudi C, Halary S, Sorzano CO, Marco S, Boudier T (2006a) TomoJ: new tools for electron tomography. In: Proceedings of the imageJ conference, 18-19 May 2006, Luxembourg
109. Messaoudi C, Loubresse NGd, Boudier T, Dupuis-Williams P, Marco S (2006b) Multiple-axis tomography: applications to basal bodies from Paramecium tetraurelia. Biol Cell 98:415-425
110. Meyer-Ilse W, Hamamoto D, Nair A, Lelievre SA, Denbeaux G, Johnson L, Pearson AL, Yager D, Legros MA, Larabell CA (2001) High resolution protein localization using soft X-ray microscopy. J Microsc 201:395-403
111. Mignot J, Brugerolle G, Didier P, Bornens M (1993) Basal-body-associated macromolecules: a continuing debate. Trends Cell Biol 3:220-223
112. Mindell JA, Grigorieff N (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142:334-347
113. Mitsuoka K, Hirai T, Murata K, Miyazawa A, Kidera A, Kimura Y, Fujiyoshi Y (1999) The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: implication of the charge distribution. J Mol Biol 286:861-882
114. Miyazawa A, Fujiyoshi Y, Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949-955
115. Mobus G, Doole RC, Inkson BJ (2003) Spectroscopic electron tomography. Ultramicroscopy 96:433-451
116. Morgan DG, Rosier DJD (1992) Processing images of helical structures: a new twist. Ultramicroscopy 46:263-285
117. Moritz M, Braunfeld MB, Guenebaut V, Heuser J, Agard DA (2000) Structure of the gamma-tubulin ring complex: a template for microtubule nucleation. Nat Cell Biol 2:365-370
118. Navaza J (2003) On the three-dimensional reconstruction of icosahedral particles. J Struct Biol 144:13-23
119. Nellist PD, Chisholm MF, Dellby N, Krivanek OL, Murfitt MF, Szilagyi ZS, Lupini AR, Borisevich A Jr, Sides W, Pennycook SJ (2004) Direct sub-angstrom imaging of a crystal lattice. Science 305:1741
120. Nicholson WV, Glaeser RM (2001) Review: automatic particle detection in electron microscopy. J Struct Biol 133:90-101
121. Nickell S, Forster F, Linaroudis A, Net WD, Beck F, Hegerl R, Baumeister W, Plitzko JM (2005) TOM software toolbox: acquisition and analysis for electron tomography. J Struct Biol 149:227-234
122. Nickell S, Kofler C, Leis AP, Baumeister W (2006) A visual approach to proteomics. Nat Rev Mol Cell Biol 7:225-230
123. O'Toole ET, Giddings TH, McIntosh JR, Dutcher SK (2003) Three-dimensional organization of basal bodies from wild-type and delta-tubulin deletion strains of Chlamydomonas reinhardtii. Mol Biol Cell 14:2999-3012
124. Owen CH, Morgan DG, Rosier DJD (1996) Image analysis of helical objects: the Brandeis helical package. J Struct Biol 116:167-175
125. Penczek P, Marko M, Buttle K, Frank J (1995) Double-tilt electron tomography. Ultramicroscopy 60:393-410
126. Penczek P, Radermacher M, Frank J (1992) Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy 40:33-53
127. Penczek PA (2002) Three-dimensional spectral signal-to-noise ratio for a class of reconstruction algorithms. J Struct Biol 138:34-46
128. Penczek PA, Frank J, Spahn CM (2006a) A method of focused classification, based on the bootstrap 3D variance analysis, and its application to EF-G-dependent translocation. J Struct Biol 154:184-194
129. Penczek PA, Grassucci RA, Frank J (1994) The ribosome at improved resolution: new techniques for merging and orientation refinement in 3D cryo-electron microscopy of biological particles. Ultramicroscopy 53:251-270
130. Penczek PA, Yang C, Frank J, Spahn CM (2006b) Estimation of variance in single-particle reconstruction using the bootstrap technique. J Struct Biol 154:168-183
131. Penczek PA, Zhu J, Frank J (1996) A common-lines based method for determining orientations for N > 3 particle projections simultaneously. Ultramicroscopy 63:205-218
132. Penczek PA, Zhu J, Schröder R, Frank J (1997) Three dimensional reconstruction with contrast transfer compensation from defocus series. Scanning Microsc 11:147-154
133. Philippsen A, Engel HA, Engel A (2007a) The contrast-imaging function for tilted specimens. Ultramicroscopy 107:202-212
134. Philippsen A, Schenk AD, Signorell GA, Mariani V, Berneche S, Engel A (2007b) Collaborative EM image processing with the IPLT image processing library and toolbox. J Struct Biol 157:28-37
135. Potter CS, Pulokas J, Smith P, Suloway C, Carragher B (2004) Robotic grid loading system for a transmission electron microscope. J Struct Biol 146:431-440
136. Provencher SW, Vogel RH (1988) Three-dimensional reconstruction from electron micrographs of disordered specimens. I. Method. Ultramicroscopy 25:209-221
137. Radermacher M (1988) Three-dimensional reconstruction of single particles from random and nonrandom tilt series. J Electron Microsc Tech 9:359-394
138. Radermacher M (1992) Weighted back-projection methods. In: Frank J (ed) Electron tomography: three-dimensional imaging with transmission electron microscope. Plenum Press, New York, pp 91-115
139. Radermacher M (1994) Three-dimensional reconstruction from random projections: orientational alignment via Radon transforms. Ultramicroscopy 53:121-136
140. Radermacher M, Rao V, Grassucci R, Frank J, Timerman AP, Fleischer S, Wagenknecht TA (1994) Cryoelectron microscopy and 3-dimensional reconstruction of the calcium release channel ryanodine receptor from skeletal-muscle. J Comput Biol 127:411-423
141. Radermacher M, Wagenknecht T, Verschoor A, Frank J (1987) Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J Microsc 146(Pt 2):113-136
142. Roseman AM (2004) FindEM-a fast, efficient program for automatic selection of particles from electron micrographs. J Struct Biol 145:91-99
143. Rosenthal PB, Henderson R (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333:721-745
144. Ruprecht JJ, Mielke T, Vogel R, Villa C, Schertler GFX (2004) Electron crystallography reveals the structure of metarhodopsin I. EMBO J 23:3609-3620
145. Saad A, Ludtke SJ, Jakana J, Rixon FJ, Tsuruta H, Chiu W (2001) Fourier amplitude decay of electron cryomicroscopic images of single particles and effects on structure determination. J Struct Biol 133:32-42
146. Saban SD, Silvestry M, Nemerow GR, Stewart PL (2006) Visualization of alpha-helices in a 6-angstrom resolution cryoelectron microscopy structure of adenovirus allows refinement of capsid protein assignments. J Virol 80:12049-12059
147. Sali A, Glaeser R, Earnest T, Baumeister W (2003) From words to literature in structural proteomics. Nature 422:216-225
148. Sander B, Golas MM, Stark H (2003) Automatic CTF correction for single particles based upon multivariate statistical analysis of individual power spectra. J Struct Biol 142:392-401
149. Saxton WO, Baumeister W (1982) The correlation averaging of a regularly arranged bacterial envelope protein. J Microsc 127:127-138
150. Scheres SH, Gao H, Valle M, Herman GT, Eggermont PP, Frank J, Carazo JM (2007) Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat Methods 4:27-29
151. Scheres SH, Marabini R, Lanzavecchia S, Cantele F, Rutten T, Fuller SD, Carazo JM, Burnett RM, San Martin C (2005a) Classification of single-projection reconstructions for cryo-electron microscopy data of icosahedral viruses. J Struct Biol 151:79-91
152. Scheres SH, Valle M, Nunez R, Sorzano CO, Marabini R, Herman GT, Carazo JM (2005b) Maximum-likelihood multi-reference refinement for electron microscopy images. J Mol Biol 348:139-149
153. Schmid MB (2001) Structural proteomics: the potential of high-throughput structure determination. Trends Microbiol 10:S27-S31
154. Sigworth FJ (1998) A maximum-likelihood approach to single-particle image refinement. J Struct Biol 122:328-339
155. Skoglund U, Ofverstedt LG, Burnett R, Bricogne G (1996) Maximum-entropy three-dimensional reconstruction with deconvolution of the contrast transfer function: a test application with adenovirus. J Struct Biol 117:173-188
156. Sorzano CO, Marabini R, Velazquez-Muriel J, Bilbao-Castro JR, Scheres SH, Carazo JM, Pascual-Montano A (2004a) XMIPP: a new generation of an open-source image processing package for electron microscopy. J Struct Biol 148:194-204
157. Sorzano COS, Fraga LGdl, Clackdoyle R, Carazo JM (2004b) Normalizing projection images: a study of image normalizing procedures for single particle three-dimensional electron microscopy. Ultramicroscopy 101:129-138
158. Sorzano COS, Jonic S, El-Bez C, Carazo JM, De Carlo S, Thevenaz P, Unser M (2004c) A multiresolution approach to orientation assignment in 3D electron microscopy of single particles. J Struct Biol 146:381-392
159. Sorzano COS, Marabini R, Boisset N, Rietzel E, Schroder R, Herman GT, Carazo JM (2001) The effect of overabundant projection directions on 3D reconstruction algorithms. J Struct Biol 133:108-118
160. Sorzano COS, Marabini R, Herman GT, Censor Y, Carazo JM (2004d) Transfer function restoration in 3D electron microscopy via iterative data refinement. Phys Med Biol 49:509-522
161. Sousa D, Grigorieff N (2007) Ab initio resolution measurement for single particle structures. J Struct Biol 157:201-210
162. Stark H, Orlova EV, Rinke-Appel J, Junke N, Muller F, Rodnina M, Wintermeyer W, Brimacombe R, van Heel M (1997) Arrangement of tRNAs in pre- and posttranslocational ribosomes revealed by electron cryomicroscopy. Cell 88:19-29
163. Subramaniam S, Milne JLS (2004) Three-dimensional electron microscopy at molecular resolution. Ann Rev Biophys Biomol Struct 33:141-155
164. Suloway C, Pulokas J, Fellmann D, Cheng A, Guerra F, Quispe J, Stagg S, Potter CS, Carragher B (2005) Automated molecular microscopy: the new Leginon system. J Struct Biol 151:41-60
165. Svergun DI, Koch MH (2002) Advances in structure analysis using small-angle scattering in solution. Curr Opin Struct Biol 12:654-660
166. Tama F, Miyashita O, Brooks CL 3rd (2004a) Flexible multi-scale fitting of atomic structures into low-resolution electron density maps with elastic network normal mode analysis. J Mol Biol 337:985-999
167. Tama F, Miyashita O, Brooks CL 3rd (2004b) Normal mode based flexible fitting of high-resolution structure into low-resolution experimental data from cryo-EM. J Struct Biol 147:315-326
168. Tao Y, Zhang W (2000) Recent developments in cryo-electron microscopy reconstruction of single particles. Curr Opin Struct Biol 10:616-622
169. Taylor KA, Glaeser RM (1974) Electron diffraction of frozen, hydrated protein crystals. Science 186:1036-1037
170. Thon F (1971) Phase contrast electron microscopy. In: Valdrè U (ed) Electron microscopy in material sciences. Academic, New York, pp 572-625
171. Thuman-Commike PA, Chiu W (1997) Improved common line-based icosahedral particle image orientation estimation algorithms. Ultramicroscopy 68:231-255
172. Thuman-Commike PA, Chiu W (2000) Reconstruction principles of icosahedral virus structure determination using electron cryomicroscopy. Micron 31:687-711
173. Toyoshima C, Unwin NTP (1988) Contrast transfer for frozen-hydrated specimens: determination from pairs of defocused images. Ultramicroscopy 25:279-292
174. Toyoshima C, Yonekura K, Sasabe H (1993) Contrast transfer for frozen-hydrated specimens II: amplitude contrast at very low frequencies. Ultramicroscopy 48:165-176
175. Unser M, Sorzano CO, Thevenaz P, Jonic S, El-Bez C, De Carlo S, Conway JF, Trus BL (2005) Spectral signal-to-noise ratio and resolution assessment of 3D reconstructions. J Struct Biol 149:243-255
176. Unser M, Trus BL, Steven AC (1987) A new resolution criterion based on spectral signal-to-noise ratios. Ultramicroscopy 23:39-51
177. Unwin P, Henderson R (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J Mol Biol 94:425-440
178. van Heel M (1982) Detection of objects in quantum-noise-limited images. Ultramicroscopy 7:331-341
179. van Heel M (1984) Multivariate statistical classification of noisy images (randomly oriented biological macromolecules). Ultramicroscopy 13:165-183
180. van Heel M (1987) Angular reconstitution: a posteriori assignment of projection directions for 3D reconstruction. Ultramicroscopy 21:111-123
181. van Heel M, Frank J (1981) Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6:187-194
182. van Heel M, Gowen B, Matadeen R, Orlova EV, Finn R, Pape T, Cohen D, Stark H, Schmidt R, Schatz M, Patwardhan A (2000) Single-particle electron cryo-microscopy: towards atomic resolution. Q Rev Biophys 33:307-369
183. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116:17-24
184. van Heel M, Schatz M (2005) Fourier shell correlation threshold criteria. J Struct Biol 151:250-262
185. van Marle J, Dietrich A, Jonges K, Jonges R, de Moor E, Vink A, Boon P, van Veen H (1995) EM-tomography of section collapse, a non-linear phenomenon. Microsc Res Tech 31:311-316
186. Velazquez-Muriel JA, Carazo JM (2007) Flexible fitting in 3D-EM with incomplete data on superfamily variability. J Struct Biol 158:165-181
187. Velazquez-Muriel JA, Sorzano CO, Fernandez JJ, Carazo JM (2003) A method for estimating the CTF in electron microscopy based on ARMA models and parameter adjustment. Ultramicroscopy 96:17-35
188. Velazquez-Muriel JA, Sorzano CO, Scheres SH, Carazo JM (2005) SPI-EM: towards a tool for predicting CATH superfamilies in 3D-EM maps. J Mol Biol 345:759-771
189. Vestergaard B, Sanyal S, Roessle M, Mora L, Buckingham RH, Kastrup JS, Gajhede M, Svergun DI, Ehrenberg M (2005) The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Mol Cell 20:929-938
190. Vogel RH, Provencher SW (1988) Three-dimensional reconstruction from electron micrographs of disordered specimens. II. Implementation and results. Ultramicroscopy 25:223-239
191. Volkmann N, Hanein D (1999) Quantitative fitting of atomic models into observed densities derived by electron microscopy. J Struct Biol 125:176-184
192. Walz T, Grigorieff N (1998) Electron crystallography of two-dimensional crystals of membrane proteins. J Struct Biol 121:142-161
193. Wang BC (1985) Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol 115:90-112
194. Wang HW, Nogales E (2005) An iterative Fourier-Bessel algorithm for reconstruction of helical structures with severe Bessel overlap. J Struct Biol 149:65-78
195. Wang L, Zhang Y, Feng J (2005) On the Euclidean distance of images. IEEE Trans Pattern Anal Mach Intell 27:1334-1339
196. Wang YA, Yu X, Yip C, Strynadka NC, Egelman EH (2006) Structural polymorphism in bacterial EspA filaments revealed by cryo-EM and an improved approach to helical reconstruction. Structure 14:1189-1196
197. White HE, Saibil HR, Ignatiou A, Orlova EV (2004) Recognition and separation of single particles with size variation by statistical analysis of their images. J Mol Biol 336:453-460
198. Yang C, Ng EG, Penczek PA (2005) Unified 3-D structure and projection orientation refinement using quasi-Newton algorithm. J Struct Biol 149:53-64
199. Zampighi GA, Zampighi L, Fain N, Wright E, Cantele F, Lanzavecchia S (2005) Conical tomography II: a method for the study of cellular organelles in thin sections. J Struct Biol 151:263-274
200. Zhang P, Beatty A, Milne JL, Subramaniam S (2001) Automated data collection with a Tecnai 12 electron microscope: applications for molecular imaging by cryomicroscopy. J Struct Biol 135:251-261
201. Zheng QS, Braunfeld MB, Sedat JW, Agard DA (2004) An improved strategy for automated electron microscopic tomography. J Struct Biol 147:91-101
202. Zhou ZH, Baker ML, Jiang W, Dougherty M, Jakana J, Dong G, Lu G, Chiu W (2001) Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus. Nat Struct Biol 8:868-873
203. Zhou ZH, Hardt S, Wang B, Sherman MB, Jakana J, Chiu W (1996) CTF determination of images of ice-embedded single particles using a graphics interface. J Struct Biol 116:216-222
204. Zhu J, Penczek PA, Schroder R, Frank J (1997) Three-dimensional reconstruction with contrast transfer function correction from energy-filtered cryoelectron micrographs: procedure and application to the 70S Escherichia coli ribosome. J Struct Biol 118:197-219
205. Zhu Y, Carragher B, Glaeser RM, Fellmann D, Bajaj C, Bern M, Mouche F, de Haas F, Hall RJ, Kriegman DJ, Ludtke SJ, Mallick SP, Penczek PA, Roseman AM, Sigworth FJ, Volkmann N, Potter CS (2004) Automatic particle selection: results of a comparative study. J Struct Biol 145:3-14
206. Zhu Y, Carragher B, Kriegman DJ, Milligan RA, Potter CS (2001) Automated identification of filaments in cryoelectron microscopy images. J Struct Biol 135:302-312
207. Ziese U, Geerts WJ, Krift TPVD, Verkleij AJ, Koster AJ (2003) Correction of autofocusing errors due to specimen tilt for automated electron tomography. J Microsc 211:179-185
208. Zubelli JP, Marabini R, Sorzano COS, Herman GT (2003) Three-dimensional reconstruction by Chahine's method from electron microscopic projections corrupted by instrumental aberrations. Inverse Probl 19:933-949